Evolution of compound eye morphology underlies differences in vision between closely related Drosophila species.

BACKGROUND: Insects have evolved complex visual systems and display an astonishing range of adaptations for diverse ecological niches. Species of Drosophila melanogaster subgroup exhibit extensive intra- and interspecific differences in compound eye size. These differences provide an excellent opportunity to better understand variation in insect eye structure and the impact on vision. Here we further explored the difference in eye size between D. mauritiana and its sibling species D. simulans. RESULTS: We confirmed that D. mauritiana have rapidly evolved larger eyes as a result of more and wider ommatidia than D. simulans since they recently diverged approximately 240,000 years ago. The functional impact of eye size, and specifically ommatidia size, is often only estimated based on the rigid surface morphology of the compound eye. Therefore, we used 3D synchrotron radiation tomography to measure optical parameters in 3D, predict optical capacity, and compare the modelled vision to in vivo optomotor responses. Our optical models predicted higher contrast sensitivity for D. mauritiana, which we verified by presenting sinusoidal gratings to tethered flies in a flight arena. Similarly, we confirmed the higher spatial acuity predicted for Drosophila simulans with smaller ommatidia and found evidence for higher temporal resolution. CONCLUSIONS: Our study demonstrates that even subtle differences in ommatidia size between closely related Drosophila species can impact the vision of these insects. Therefore, further comparative studies of intra- and interspecific variation in eye morphology and the consequences for vision among other Drosophila species, other dipterans and other insects are needed to better understand compound eye structure-function and how the diversification of eye size, shape, and function has helped insects to adapt to the vast range of ecological niches.

Proprioception gates visual object fixation in flying flies.

Visual object tracking in animals as diverse as felines, frogs, and fish supports behaviors including predation, predator avoidance, and landscape navigation. Decades of experimental results show that a rigidly body-fixed tethered fly in a "virtual reality" visual flight simulator steers to follow the motion of a vertical bar, thereby "fixating" it on visual midline. This behavior likely reflects a desire to seek natural features such as plant stalks and has inspired algorithms for visual object tracking predicated on robust responses to bar velocity, particularly near visual midline. Using a modified flight simulator equipped with a magnetic pivot to allow frictionless turns about the yaw axis, we discovered that bar fixation as well as smooth steering responses to bar velocity are attenuated or eliminated in yaw-free conditions. Body-fixed Drosophila melanogaster respond to bar oscillation on a stationary ground with frequency-matched wing kinematics and fixate the bar on midline. Yaw-free flies respond to the same stimulus by ignoring the bar and maintaining their original heading. These differences are driven by proprioceptive signals, rather than visual signals, as artificially "clamping" a bar in the periphery of a yaw-free fly has no effect. When presented with a bar and ground oscillating at different frequencies, a yaw-free fly follows the frequency of the ground only, whereas a body-fixed fly robustly steers at the frequencies of both the bar and ground. Our findings support a model in which proprioceptive feedback promote active damping of high-gain optomotor responses to object motion.

Acuity and summation strategies differ in vinegar and desert fruit flies.

An animal's vision depends on terrain features that limit the amount and distribution of available light. Approximately 10,000 years ago, vinegar flies (Drosophila melanogaster) transitioned from a single plant specialist into a cosmopolitan generalist. Much earlier, desert flies (D. mojavensis) colonized the New World, specializing on rotting cactuses in southwest North America. Their desert habitats are characteristically flat, bright, and barren, implying environmental differences in light availability. Here, we demonstrate differences in eye morphology and visual motion perception under three ambient light levels. Reducing ambient light from 35 to 18 cd/m2 causes sensitivity loss in desert but not vinegar flies. However, at 3 cd/m2, desert flies sacrifice spatial and temporal acuity more severely than vinegar flies to maintain contrast sensitivity. These visual differences help vinegar flies navigate under variably lit habitats around the world and desert flies brave the harsh desert while accommodating their crepuscular lifestyle.

Prenatal incubation temperature affects neonatal precocial birds' locomotor behavior.

Temperature during the prenatal period is an important factor for developing embryos. Extensive human and animal research indicate embryos are sensitive to small fluctuations in temperature which has profound effects on phenotype development. Much of this research has focused on survivability, morphology, and incubation duration, but comparatively less in known about how prenatal temperature influences the development of motor coordination. In this study, we experimentally tested whether exposure to naturally occurring cool (36.9 °C) or warm (38.1 °C) thermal conditions for a brief period (4 days) during early incubation can influence postnatal motor performance in neonatal bobwhite quail hatchlings. We compared gait spatiotemporal parameters, body kinematics, and locomotive behaviors of control chicks incubated in an optimal thermal environment (37.5 °C) with thermally manipulated chicks. Experimental temperature treatment began on embryonic day five (E5) and ended on E8. Chicks were tested 24-h after hatching. Cool thermal exposure during incubation delayed hatching, reduced body mass, and increased fall frequency, intertarsal joint angle and stride length variability during the gait task compared to optimally incubated chicks. Warm thermal exposure during incubation delayed bone growth and increased fall frequency relative to controls. We discuss the relationship between motor development and thermal regulatory processes and provide insight into how spatiotemporal parameters aid in elucidating subtle differences in coordinated movement which may contribute to atypical motor development and be associated with neural developmental disorders. We provide the first spatiotemporal evidence for the importance of optimal thermal microclimates for typical prenatal motor development.

Small fruit flies sacrifice temporal acuity to maintain contrast sensitivity.

Holometabolous insects, like fruit flies, grow primarily during larval development. Scarce larval feeding is common in nature and generates smaller adults. Despite the importance of vision to flies, eye size scales proportionately with body size, and smaller eyes confer poorer vision due to smaller optics. Variable larval feeding, therefore, causes within-species differences in visual processing, which have gone largely unnoticed due to ad libitum feeding in the lab that results in generally large adults. Do smaller eyes have smaller ommatidial lenses, reducing sensitivity, or broader inter-ommatidial angles, reducing acuity? And to what extent might neural processes adapt to these optical challenges with temporal and spatial summation? To understand this in the fruit fly, we generated a distribution of body lengths (1.67-2.34 mm; n = 24) and eye lengths (0.33-0.44 mm; n = 24), resembling the distribution of wild-caught flies, by removing larvae from food during their third instar. We find smaller eyes (0.19 vs.0.07 mm2) have substantially fewer (978 vs. 540, n = 45) and smaller ommatidia (222 vs. 121 µm2;n = 45) separated by slightly wider inter-ommatidial angles (4.5 vs.5.5°; n = 34). This corresponds to a greater loss in contrast sensitivity (<50%) than spatial acuity (<20%). Using a flight arena and psychophysics paradigm, we find that smaller flies lose little spatial acuity (0.126 vs. 0.118CPD; n = 45), and recover contrast sensitivity (2.22 for both; n = 65) by sacrificing temporal acuity (26.3 vs. 10.8Hz; n = 112) at the neural level. Therefore, smaller flies sacrifice contrast sensitivity to maintain spatial acuity optically, but recover contrast sensitivity, almost completely, by sacrificing temporal acuity neurally.